Interpretive Summary: Sunflower is one of the few crop species that is native to North America. This affords the opportunity for exchange of genes between the cultivated crop and its wild ancestors. Hybrids between cultivated and wild sunflower are frequently reported suggesting that transgenes in cultivated sunflower could introgress into wild sunflower populations. This study looks at gene flow from cultivated sunflowers and their genetic structure and persistence up to 40 years in wild sunflower populations. Persistent, long term gene flow in sunflower can lead to high levels of crop-wild introgression. The selected molecular markers from the cultivated sunflower were found in nearly all plants of the wild populations demonstrating a high rate of introgression between cultivated and wild sunflowers and that pure wild plants in these populations have been replaced by plants of hybrid ancestry. These results clearly demonstrate the high probability that transgenes will flow into wild sunflower populations. However, the escape and spread of transgenes in sunflower and other crops will largely depend on fitness consequences and linkage relationships of individual transgenes in a wild-type genetic background rather than overall hybrid fitness.

Technical Abstract:
Hybrids between cultivated and wild sunflowers (Helianthus annuus) are frequently reported, suggesting that transgenes in cultivated sunflowers could introgress into wild sunflower populations. Recent studies have shown that up to 42% of progeny from wild plants near cultivar fields are hybrids, that first generation hybrids have only slightly lower fitness than purely wild plants, and that cultivar genes can persist in wild populations up to five generations following the initial hybridization event. Here, we extend these studies by describing the effects of up to 40 years of persistent cultivar gene flow on the genetic structure of three wild H. annuus populations that were adjacent to cultivated fields. We also provide the first comprehensive study in which the patterns of introgression of multiple genetically-mapped markers are determined. Use of mapped markers allowed us to distinguish between symplesiomorphy and introgression and ensured adequate genomic coverage. Surveys of 18 cultivar-specific markers in a total of 115 individuals from three sympatric wild populations revealed high rates of cultivar marker frequencies. Population means for introgressed marker frequencies ranged from 0.315 to 0.382. All 115 plants had at least one cultivar marker, suggesting that all or nearly all wild plants in these populations have a hybrid ancestor. Thus, persistent, long-term gene flow in sunflowers can lead to high levels of crop-wild introgression. Only crop-specific markers that were physically linked showed significant linkage disequilibrium. Overall our results indicate that individual cultivar genes will introgress into wild sunflowers independently from other cultivar genes as long as they are not tightly linked.